Journal of Mammalogy, 90(2):332–339, 2009
DIFFERENCES IN THE COMPOSITION OF COLOSTRUM AND
MILK IN EUTHERIANS REFLECT DIFFERENCES IN
IMMUNOGLOBULIN TRANSFER
PETER LANGER*
Institut für Anatomie & Zellbiologie, Justus-Liebig-Universität, Aulweg 123, D-35385 Giessen, Germany
Colostrum is a special type of milk produced in eutherian mammals during the end of pregnancy and during the
1st few days after birth. It supplies passive immunity to the offspring. The composition of colostrum and mature
milk is compared in this study. In species with prenatal passive immunization (humans, baboons, and rabbits),
immunoglobulin transfer via colostrum is of little importance and the difference in relative protein concentration
between colostrum and mature milk can be small. In ungulates, on the other hand, colostrum has to supply the
offspring postnatally with passive immunity and colostrum is relatively rich in immunoglobulin. Large
differences between relative protein concentration in colostrum and milk can be observed in ungulates.
Compositions of colostrum and milk thus reflect differences in immunoglobulin transfer.
Key words:
carbohydrate, colostrum, fat, mature milk, passive immunity, protein
of this latter function, protein cannot be replaced by fat and
carbohydrate, which supply energy needed for metabolism.
A large part of the high protein percentage in colostrum
‘‘is due to the globulin contents that contain the antibodies’’
(Park 2006b:394). For example, in pigs (Sus scrofa) 55% of the
total crude protein consists of immunoglobulins (Pluske et al.
1995). Although Lascelles (1979) states that concentrations of
immunoglobulin in the colostrum of eutherian species are high
compared with those detected in mature milk, this statement
cannot be generalized. For example, in some species (e.g., in
the orders Primates, Rodentia, Lagomorpha, and Proboscidea)
protein represents ,50% of the nutrients in their colostrum,
whereas others (e.g., Cetacea and Artiodactyla—particularly
Camelidae, Suidae, and many Ruminantia) show a high percentage of protein. On the other hand, mature milk of different
eutherian species contains ,50% protein, which is consistent
with data published by Braun (1997).
Thus, in some species colostrum can contain higher concentrations of protein than mature milk, but in other species similar
compositions exist in both liquids. Differences in the composition of colostrum and milk in eutherians may reflect different
species-specific strategies for immunoglobulin transfer. This
study examines this hypothesis using data compiled from the
literature on protein, fat, and carbohydrate concentration in
colostra and milks.
Newborn mammals encounter a microbially hostile environment. Response to this situation affords passive immunization
either by prenatal transfer of immunoglobulins via placenta or
yolk sac or by postnatal transport of immunoglobulin from
mother to offspring via colostrum (Baintner 2007). Differences
in protein transfer from mother to offspring among eutherian
species are considerable (Vernier and Sire 1981). In hoofed
mammals, transfer of immunoglobulins via the epitheliochorial
placenta does not take place and the fetus acquires few or no
antibodies across the placental barrier (Baintner 2007; Gaskin
and Kelley 1995). This multicellular obstacle consists not only
of layers of maternal endometrium, but also of fetal chorion.
However, postnatally immunoglobulins are supplied by
absorption from colostrum via the gut wall (Lascelles 1979).
During the very 1st days after birth, the newborn ungulate is
essentially devoid of circulating antibodies until absorption
from the colostrum is possible. The animals are born in
a ‘‘hypogammaglobulinaemic state’’ (Baintner 2007:159).
Colostrum is a special type of milk formed during the last
days of pregnancy and in the 1st few days after birth. In some
mammals, especially ungulates, colostrum is particularly rich
in proteins. Protein contributes to the synthesis of cells and
tissues and to the formation of enzymes and antibodies
(immunoglobulin G [IgG], IgA, and IgM). Especially because
MATERIALS AND METHODS
* Correspondent: [email protected]
This paper compares the composition of colostrum with that
of mature milk. The comparison is based on data from the
literature that were published between 1962 and 2006. In these
Ó 2009 American Society of Mammalogists
www.mammalogy.org
332
April 2009
LANGER—COLOSTRUM, MILK, AND PASSIVE IMMUNITY
333
TABLE 1.—Contents of nutrients (proteins, fats, and carbohydrates) in colostrum of 19 eutherian species. Units of measure and references are
also given. Scientific names of species follow Wilson and Reeder (2005). Data with different units of measure are given in the literature for the pig
(Sus scrofa). Therefore, 2 data sets are given for this species. In all other species means could be calculated because identical dimensions were
given. These means are listed in the table.
Colostrum nutrients
Species
Homo sapiens
Papio
Canis lupus
Felis catus
Balaena mysticetus
Loxodonta africana
Equus caballus
Sus scrofa
Sus scrofa
Pecari tajacu
Camelus dromedaries
Camelus bactrianus
Lama glama
Mazama gouazoubira
Bos taurus
Bos grunniens
Ovis aries
Capra hircus
Rattus norvegicus
Oryctolagus cuniculus
Human
Baboon
Dog
Cat
Bowhead whale
African elephant
Horse
Pig
Pig
Collared peccary
Dromedary
Bactrian camel
Llama
Mazama deer
Cow
Yak
Sheep
Goat
Rat
Rabbit
Protein
Fat
Carbohydrate (lactose)
Unit
Reference
22.9
2.3
138.0
4.0
86.6
21.0
191.0
180.0
10.6
6.0
13.0
19.2
16.5
95.2
130.0
16.1
130.0
80.0
8.9
135.0
29.5
5.1
78.0
3.4
4.9
56.0
7.0
72.0
5.8
4.8
1.5
0.3
1.0
87.0
36.0
14.0
124.0
90.0
14.7
147.0
57.0
6.8
27.0
3.6
6.3
61.8
46.0
24.0
3.4
5.2
3.6
5.9
6.3
11.1
31.0
1.9
34.0
25.0
2.5
16.0
g/l
g/100 ml
g/kg
%
%
g/kg
g/kg
g/kg
%
%
%
%
%
g/dl
g/kg
%
g/kg
g/kg
%
g/kg
Documenta Geigy (1969)
Buss (1968)
Meyer and Kamphues (1990)
Keen et al. (1982)
Harms (1993)
Osthoff et al. (2005)
Meyer and Kamphues (1990)
Meyer and Kamphues (1990)
Park (2006a)
Sowls (1984)
Abu Lehia et al. (1989), El-Agamy (2006)
El-Agamy (2006)
Rosenberg (2006)
Fernández et al. (1999)
Meyer and Kamphues (1990)
Silk et al. (2006)
Meyer and Kamphues (1990)
Meyer and Kamphues (1990)
Keen et al. (1981)
Meyer and Kamphues (1990)
publications quantities of protein, fat, and carbohydrate are
expressed in different dimensions, either in grams per weight,
grams per volume, or percentages of total liquid volume. They
can be pooled by considering their sum, independent of their
original dimensions, as protein þ fat þ carbohydrate ¼ 100%.
When this is done both for colostrum and mature milk, the
differences in protein, fat, and carbohydrate percentages
between both liquids (percent colostrum percent milk) can
be determined for different eutherian species. When .1
measurement for either colostrum or mature milk per species
was available, means were used. Originally, 36 measurements
from 20 eutherian species were available for composition of
colostrum, and 137 measurements from 60 species for
composition of mature milk. Data were compiled as triangular
(or ternary) diagrams, which present percentages of fats,
proteins, and carbohydrates for colostrum and for mature milk.
Raw data are not listed in this paper, but can be obtained from
the author upon request.
Some authors, for example, El-Agamy (2006), supplied
results of .1 measurement. These were not considered
separately, but means are given for those measurements
presented in identical dimensions. However, data for the
colostrum of pigs (S. scrofa) and for mature milk of house cats
(Felis catus) and pigs were sometimes presented in different
dimensions and are therefore considered separately. Dimensions can either be grams per weight, grams per volume, or
percentages of total liquid volume. They can be pooled by
considering their sum, independent of their original dimensions, as protein þ fat þ carbohydrate ¼ 100%. Comparisons
of the composition of colostrum and mature milk were thus
based on 19 eutherian species (Tables 1 and 2).
To characterize and compare the composition of colostrum
and milk from eutherian species for which measurements of
both were available, their concentrations of protein, fat, and
carbohydrate were compiled from the literature. Assuming that
immunoglobulin transfer from mother to offspring is an
important factor influencing the composition of colostrum,
only those species were considered where information on
immunoglobulin transfer was clearly reported (Baintner 2007)
or where ‘‘informed guesses,’’ based on closely related species
(see below), could be made. In many species, the carbohydrates
in secretions of the mammary gland are primarily in the form of
lactose (Karasov and Martı́nez del Rio 2007). When only data
on lactose concentration were given in references, this was
taken as representing the total concentration of carbohydrate in
colostrum or milk.
Data on milk composition taken from the literature present
a problem because mature milk can change in composition
during the lactation period (Oftedal 1984). In most of the
references ‘‘peak lactation’’ is the time when measurements
were made, but in free-ranging wild mammals, such as Balaena
mysticetus (bowhead whale), Loxodonta africana (African
elephant), or Pecari tajacu (collared peccary), clear statements
concerning the lactation stages were not made.
Colostrum changes in carbohydrate, fat, and protein composition during the 1st days of postnatal life (Baintner 2007),
becoming more and more similar to mature milk. It was problematic to obtain unambiguous, well-defined data on colostrum
for all eutherian species included in the analyses. Many data
were taken from review volumes (e.g., Meyer and Kamphues
1990; Park 2006a) to base this survey on generally accepted
information and to obtain comparable data for .1 eutherian
334
Vol. 90, No. 2
JOURNAL OF MAMMALOGY
TABLE 2.—Contents of nutrients (proteins, fats, and carbohydrates) in mature milk of 19 eutherian species. Units of measure and references are
also given. Scientific names of species follow Wilson and Reeder (2005). Data with different units of measure are given in the literature for the cat
(Felis catus) and the pig (Sus scrofa). Therefore, 2 data sets are given for these species. In all other species means could be calculated because
identical dimensions were given. These means are listed in the table.
Mature milk nutrients
Species
Homo sapiens
Papio
Canis lupus
Felis catus
Felis catus
Balaena mysticetus
Loxodonta africana
Equus caballus
Sus scrofa
Sus scrofa
Pecari tajacu
Camelus dromedarius
Camelus bactrianus
Lama glama
Mazama gouazoubira
Bos taurus
Bos grunniens
Ovis aries
Capra hircus
Rattus norvegicus
Oryctolagus cuniculus
Human
Baboon
Dog
Cat
Cat
Bowhead whale
African elephant
Horse
Pig
Pig
Collared peccary
Dromedary
Bactrian camel
Llama
Mazama deer
Cow
Yak
Sheep
Goat
Rat
Rabbit
Protein
Fat
Carbohydrate (lactose)
Unit
Reference
10.6
1.6
80.0
55.0
6.6
9.4
25.0
25.0
51.0
5.1
5.3
3.3
4.2
5.0
65.0
33.0
5.3
58.0
30.0
12.1
127.0
45.4
5.0
90.0
48.0
5.5
19.4
76.0
20.0
79.0
5.4
4.6
4.1
5.3
5.5
48.2
38.0
7.0
60.0
34.0
12.2
148.0
71.0
7.3
30.0
40.0
4.1
0.0
18.9
65.0
52.0
5.7
6.5
4.4
4.9
6.6
55.3
50.0
4.6
43.0
45.0
2.5
9.0
g/l
g/100 ml
g/kg
g/kg
%
%
g/kg
g/kg
g/kg
%
%
%
%
%
g/dl
g/kg
%
g/kg
g/kg
%
g/kg
Documenta Geigy (1969)
Buss (1968)
Meyer and Kamphues (1990)
Meyer and Kamphues (1990)
Keen et al. (1982)
Ben Shaul (1962)
Osthoff et al. (2005)
Meyer and Kamphues (1990)
Meyer and Kamphues (1990)
Park (2006a)
Sowls (1984), Lochmiller et al. (1985)
Abu Lehia et al. (1989), El-Agamy (2006)
El-Agamy (2006)
Rosenberg (2006)
Fernández et al. (1999)
Meyer and Kamphues (1990)
Silk et al. (2006)
Meyer and Kamphues (1990)
Meyer and Kamphues (1990)
Keen et al. (1981)
Meyer and Kamphues (1990)
species. In 3 species (cow [Bos taurus], sheep [Ovis aries], and
goat [Capra hircus]) domestication produced races specialized
either on milk, meat, wool, or multipurpose production. These
breeds might produce colostrum and milk of various
compositions, which were not taken into account in the present
general survey. The present study is—to the knowledge of the
author—the 1st that compares colostrum and milk under
consideration of different strategies of passive immunization.
Information determined under controlled and reproducible
conditions could not be obtained for all eutherian species
included in the analyses, but data of suboptimal quality can still
produce valuable insights.
RESULTS
Concentrations of fats, protein, and carbohydrates varied
considerably among species in both colostrum (Fig. 1a) and
mature milk (Fig. 1b). Variation in the concentration of protein
FIG. 1.—Two triangular or ternary diagrams representing composition of fats, proteins, and carbohydrates in a) colostrum and b) mature milk;
36 measurements from 20 eutherian species were available for colostrum and 137 measurements from 60 species for mature milk. The sum of
protein plus fat plus carbohydrate is considered as 100%. The percentage of protein can be read from the bottom line of the triangle (0%) to the top
corner (100%). The percentage of fat starts at the upper right (0%) and ends at the lower left corner (100%). The percentage of carbohydrate is read
from top left to bottom right corner. Dotted lines mark 25%, 50%, and 75%.
April 2009
LANGER—COLOSTRUM, MILK, AND PASSIVE IMMUNITY
335
FIG. 2.—a) Differences between the relative concentration of proteins (expressed as percent of protein þ fat þ carbohydrate ¼ 100%) in
colostrum and mature milk for 19 eutherian species. Comparable diagrams are presented for b) fats and c) carbohydrates. Species names are
provided in Tables 1 and 2. Positive values mean higher concentrations in colostrum than in mature milk. When concentrations in colostrum are
smaller than in mature milk, the columns lie in the negative range. Three types of the maternal–fetal immunoglobulin transfer are indicated by
different fill patterns. Question marks indicate taxa for which no unambiguous information on maternal–fetal transfer was available. Number signs
(#) indicate taxa for which it is not clearly documented whether transfer happens pre- or postnatally. ‘‘Informed guesses’’ were extrapolated from
information on closely related eutherian species, where transfer can be observed either prenatally via the placenta or the yolk-sac wall, or
postnatally from colostrum via the small intestine. For example, Mazama deer have not been investigated in this respect, but in other artiodactyls
immunoglobulins are supplied to the newborn postnatally (Baintner 2007; Lascelles 1979).
336
JOURNAL OF MAMMALOGY
was particularly pronounced in the data examined for colostrum. For example, protein concentration in the colostrum (in g/kg)
of horses (Equus caballus) and pigs was similar, but colostra
of these species were highly different in concentrations of fat
and carbohydrate. When milks of the 2 species are compared,
protein and fat concentrations varied considerably between
species. Differences in percentages of protein, fats, and
carbohydrates between colostrum and mature milk (percent
colostrum percent milk) were calculated for the 19 eutherian
species, and related to the pattern of postnatal transfer of antibodies (proteins) from mother to young (Fig. 2). In the figure,
species with prenatal, with pre- as well as postnatal, and with
postnatal transfer of immunoglobulin form 3 groups. In
general, the colostrum of species with postnatal transfer of
immunoglobulins has a much greater proportion of protein
than the mature milk of those species (Fig. 2a).
Oftedal (1984) demonstrated that milk composition varies
considerably over the course of the lactation period, but many
of the data presented here are based on very few analyses
and, because of this, have little information about the state of
lactation when milk samples were taken (Park and Haenlein
2006). Data listed in Tables 1 and 2 represent ‘‘averages’’ taken
from different sources and obtained from different authors with
different methods. Thus, patterns are discussed qualitatively.
An ideal comparison would consider colostrum and milk from
the same mother during ontogeny of her young—data that were
not available in the present study. A statistical comparison of
few data from very different sources would suggest greater
precision than can be offered by presently available data.
DISCUSSION
Differences in the composition of colostrum and milk in the
19 species of eutherians examined in this study reflected
differences in immunoglobulin transfer. All newborn mammals, including humans (Homo sapiens), are exposed to an
environment rich in antigens. Without passive transfer of
antibodies from the mother, most ‘‘trivial’’ infections would
be dangerous in this early phase of life (Braun 1997;
Buschmann 1990). The offspring is dependent on the
transmission of maternal antibodies (Malek 2003). In colostrum, a large proportion of the protein is globulin that
contains antibodies (Park 2006b). Postnatally, proteins, fats,
and carbohydrates together contribute to build up body mass
and to differentiate tissues and cells. Proteins, fats, and
carbohydrates combined represent .90% of solids in milk
(Park and Haenlein 2006).
Before reaching full immunocompetence, newborn mammals are protected from infections by maternal antibodies that
enable passive immunity. To accomplish this, 3 routes may be
used (Baintner 2007; Butler 1974): transfer from mother to
fetus through the chorioallantoic placenta may occur; transfer
via the yolk-sac wall may occur; or IgG is absorbed from the
colostrum via the intestinal wall, mainly the ileum (Baintner
2007). In this latter case, antibodies are not destroyed during
the first 24 h of life of the newborn, but with increasing
intensity of the digestive process most immunoglobulins are
Vol. 90, No. 2
digested in the offspring’s gut. In newborn kittens, maximum
IgG concentration in blood serum is reached on day 2 after
parturition (Claus et al. 2006), which means that colostrum is
ingested by the newborn before that day. In naturally suckling
piglets, on the other hand, the period of production of colostrum seems to be longer, because they begin to synthesize their
own IgG as late as 7 days of age (Rooke et al. 2003).
Prenatal transfer of immunity from mother to fetus via the
placenta is mainly accomplished by immunoglobulins of the
IgG class (Herrmann and Forstreuter 1967; Lin 1980; Vernier
and Sire 1981), which provide the newborn with sufficient
passive immunity against infectious pathogens until the
neonatal immune system has matured (Malek 2003). On the
other hand, Merad and Wild (1992) emphasized that the rabbit
(Oryctolagus cuniculus) fetus acquires passive immunity not
only in the form of maternal IgG, but also by maternal IgM.
Both immunoglobulins are transported prenatally to the fetal
blood.
Prenatal transfer of maternal antibodies depends on the
architecture of the barrier between mother and fetus. IgG is
a relatively small molecule suited for vesicular transport
through the trophoblast barrier of the human hemochorial
placenta (Kaufmann 1990; Mossman 1987). In this placental
type, maternal immunoproteins can be transferred directly into
the blood of the offspring, which enables passive immunological protection. In humans, immunoglobulins have to pass
the placenta, which has only the syncytiotrophoblast as the
important transport barrier (Lüllmann-Rauch 2003). Passage
of IgG through this barrier takes place via transcytosis
(Lüllmann-Rauch 2003; Welsch 2003), which requires
immunoglobulin-binding proteins, the ‘‘Fc receptors,’’ involved in antibody transport (Jenkinson et al. 1976; Kacskovics
2004). As an effect of this, there is no significant postnatal
immunoglobulin absorption from the gut of newborn humans
(Baintner 2007).
In the representatives of rodents and lagomorphs examined
to date (Rattus, Mus, and Oryctolagus), maternal c-globulin is
transferred to the fetal blood via the yolk-sac wall (Brambell
et al. 1948; Brambell and Halliday 1956). Regardless of the
route—yolk-sac wall or placenta—it is well established that
immunoglobulin is transferred to the fetal circulation (Elson
et al. 1975).
As can be seen in Fig. 2a, prenatal transfer of immunoglobulin in humans, baboons (Papio), and rabbits is related to
relatively small differences in protein concentration between
colostrum and mature milk. Concentrations of fats (Fig. 2b)
and carbohydrates (Fig. 2c) in colostrum and milk also do not
differ greatly. On the other hand, most ungulate species with
postnatal globulin transfer produce colostrum that is much
richer in protein than mature milk (Fig. 2a). In these cases,
especially in ungulates, passive immunization of the offspring
takes place immediately after birth via this rich colostrum.
The greater protein concentration in the colostrum than in
milk of ungulates is related to the fact that ungulates produce
precocial young that ‘‘subsidize’’ their mothers in the final
phase of lactation by searching for and eating solid food
(Langer 2008a, 2008b). In 4 species with postnatal immuno-
April 2009
LANGER—COLOSTRUM, MILK, AND PASSIVE IMMUNITY
globulin transfer (collared peccaries, Mazama deer [Mazama
gouazoubira], sheep, and goats) differences in protein
concentration between colostrum and mature milk are relatively small. In the majority of ungulates, milk is richer in fats
and carbohydrates than is colostrum (Figs. 2b and 2c); fats
and carbohydrates both supply energy to the young offspring.
Recent research demonstrated that ‘‘cetaceans are highly
derived artiodactyls’’ (Milinkovitch et al. 1998), a statement
that is well accepted among mammalogists (Berta and Sumich
1999; Geisler and Luo 1998). Under these circumstances it is
justified to assume that the time of immunoglobulin transfer
takes place postnatally in cetaceans, although unambiguous
information on this subject is not available. In the bowhead
whale, carbohydrate concentration was higher in colostrum
than in milk (Fig. 2c), which is different from the situation in
Artiodactyla. On the other hand, the greater fat concentration in
mature milk than colostrum of Balaena mysticetus might be
due to metabolic needs of the growing cetacean offspring.
According to Baintner (2007), the rat (Rattus norvegicus;
Rodentia) and the dog (Canis lupus; Carnivora) show
immunoglobulin transfer pre- and postnatally. Stoffel et al.
(2000) discuss transport of IgG via the placenta of female dogs.
Relative protein concentration is higher in colostrum than in
milk of dogs, whereas the milk of rats contains relatively more
protein than does colostrum. The latter statement can also be
made for the cat, a carnivoran. In his extensive study, Braun
(1997) corroborates this observation. He stated that protein
concentration increases from colostrum to mature milk in
rodents and cats, and also in lagomorphs. In rabbits, which
show exclusive prenatal transfer of protein from mother to
offspring (Baintner 2007), the difference between relative
protein concentration in colostrum and milk is minute, as are
the differences in relative fat and carbohydrate concentrations.
Because of prenatal transfer, young of rabbits do not need
a colostrum that is considerably different from mature milk.
Because they are born in a very altricial condition, it is important that the quality of the food supplied by the mother is
high, the phase when milk is the only food ingested by the
young animal is relatively long, and the time when milk and
solid food are taken represents a relatively short time of
transition to adult feeding conditions (Langer 2008b).
It is frustrating that the following question cannot be
answered: Why is the percentage of protein in milks of cats,
African elephants, and rats higher than in colostrum? At least
for the data used here for domestic cats it is highly improbable
that the colostrum produced immediately after birth was not
clearly separated from the milk produced later. Very probably,
the increase in protein percentage from colostrum to milk is not
an artifact, because it was possible to calculate from data
published by Day (2007) that absolute immunoglobulin content
is considerably lower (8.3 mg/ml) in feline colostrum than in
mature milk (19.1 mg/ml). Braun (1997) documented an
increase in protein percentage from colostrum to milk, but
a clear explanation for this deviation from other carnivores
could not be given by that author. On the other hand, he
mentions that colostrum is richer in protein than the milk in
other species of Carnivora.
337
It is possible that the data listed for the African elephant in
Table 1 may not really refer to colostrum. Osthoff et al. (2005)
collected milk samples from an African elephant cow covering
the period from the 4th day after birth onward. In addition,
unambiguous information on immunoglobulin transfer in L.
africana is not available.
The small differences between colostrum and mature milk in
protein concentration in collared peccaries and Mazama deer
could be due to ambiguous information in the literature, but no
clear explanation for why these species differ quantitatively
from the other ungulates examined can be given. Small
differences in protein concentrations of colostrum and mature
milk also were found for domestic sheep, although careful and
controlled measurements (Meyer and Kamphues 1990) were
possible in this species.
In future investigations the above-mentioned uncertainties
could be resolved if colostrum and mature milk from the same
mother during the same lactation period were evaluated in as
many eutherian species as possible. In spite of the possible bias
from suboptimal data that were available for some species in
this study, 3 conclusions can be drawn about why colostrum and
milk composition are different in some species (e.g., ungulates)
and similar in others (primates, rodents, and lagomorphs).
Data for 3 species with prenatal immunoglobulin transfer
were available in this study (humans, baboons, and rabbits).
Prenatal transfer of immunoglobulins was associated with
small differences between the relative concentration of proteins
in colostrum and milk. Differences in percentages of fats and
carbohydrates between colostrum and mature milk also were
small. Because of prenatal passive immunization via the
placenta in humans and baboons, or via the Fc-receptor in the
everted yolk sac in rabbits (Baintner 2007), the postnatal
transfer of protein from mother to offspring can be relatively
low and a considerable change in composition from colostrum
to milk is not necessary.
Two carnivores (dogs and cats) and 1 rodent (rats) examined
in this study transfer immunoglobulins pre- and postnatally
(Baintner 2007). In these 3 species, the differences in relative
percentages of proteins, fats, and carbohydrates were low, that
is, colostrum and milk did not differ considerably. The prenatal
part of immunoglobulin transfer will, very probably, reduce the
importance of postnatal transfer. More data should be available
for species with pre- and postnatal phases of transfer to obtain
a clear picture of the relationship between composition of
colostrum and milk.
When prenatal maternal–fetal transfer of immunoglobulin is
inhibited, such as in ungulates, colostrum has to boost immune
protection of the newborn, which means that immunoglobulin
has to be available postnatally in great quantities. In this
situation, large differences can be observed between relative
protein concentration of colostrum and mature milk. This has
the consequence that the differences for fat and carbohydrate
are also high in species with postnatal globulin transfer. In most
of these species, fats and carbohydrates are relatively more
important in mature milk than in colostrum. With increasing
age and change from colostrum to mature milk, the young
animal develops its own immune protection and the relative
338
JOURNAL OF MAMMALOGY
amount of immunoglobulins and proteins in general decreases
from colostrum to milk.
ZUSAMMENFASSUNG
Kolostrum ist ein besonderer Typ Milch, der von den
Eutheria am Ende der Trächtigkeit und in den ersten Tagen
nach der Geburt gebildet wird und passive Immunität gegen
schädliche Keime vermittelt. Warum unterscheiden sich die
relativen Proteingehalte von Kolostrum und Milch bei
verschiedenen Arten? Die Rohdaten zur Beantwortung dieser
Frage wurden für 19 Eutheria-Arten aus der Literatur
zusammengestellt und der Proteingehalt für Kolostrum und
Milch wird ausgedrückt als Prozent der Summe der Nährstoffe
(Protein þ Fett þ Kohlenhydrat ¼ 100%). Vor der Geburt wird
beim Menschen, Pavian und Kaninchen Protein, welches zum
großen Teil aus Immunglobulinen besteht, entweder über die
Plazenta oder andererseits über die Wand des Dottersacks von
der Mutter in den Blutkreislauf des Nachkommen transportiert.
Bei Huftieren wird nach der Geburt Protein, und damit auch
Immunglobulin, über das vom Jungtier aufgenommene Kolostrum durch die Darmwand resorbiert. Wenn passive Immunität
vor der Geburt erzielt wird, ist der Transfer von Immunglobulinen über Kolostrum von geringer Bedeutung, was zur
Folge hat, dass sich die relativen Proteingehalte von Kolostrum
und reifer Milch nur wenig unterscheiden. Andererseits wird
bei Huftieren nach der Geburt das Neugeborene über das
Kolostrum mit reichlich Immunglobulinen versorgt und der
Unterschied der Proteingehalte von Kolostrum und Milch ist
groß. Die Befunde zeigen, dass die Differenzen in der
Zusammensetzung von Kolostrum und Milch die Unterschiede
im Zeitpunkt der passiven Immunisierung wiederspiegeln.
ACKNOWLEDGMENTS
R. Leiser (previously of Institut für Veterinär-Anatomie, Histologie
und Embryologie, Justus-Liebig-Universität, Giessen, Germany)
supplied literature on placental architecture and C. Kunz (Institut für
Ernährungswissenschaft der Justus-Liebig-Universität, Giessen) provided information about literature on milk composition of mammals.
Two anonymous reviewers offered constructive and very helpful
criticism. The efforts of these colleagues are greatly appreciated. R. L.
Snipes (previously of Institut für Anatomie & Zellbiologie, JustusLiebig-Universität, Giessen) reviewed and improved the English, for
which I owe him—as so often before—gratitude.
LITERATURE CITED
ABU LEHIA, I. H., I. S. AL MOHIZEA, AND M. EL BEHERI. 1989. Physical
and chemical characteristics of camel colostrum. Australian Journal
of Dairy Technology 44:34–36.
BAINTNER, K. 2007. Transmission of antibodies from mother to young:
evolutionary strategies in a proteolytic environment. Veterinary
Immunology and Immunopathology 117:153–161.
BEN SHAUL, D. M. 1962. The composition of the milk of wild animals.
International Zoo Yearbook 4:333–342.
BERTA, A., AND J. L. SUMICH. 1999. Marine mammals: evolutionary
biology. Academic Press, San Diego, California.
BRAMBELL, F. W. R., AND R. HALLIDAY 1956. The route by which
passive immunity is transmitted from mother to foetus in the rat.
Vol. 90, No. 2
Proceedings of the Royal Society of London, B. Biological Sciences
145:170–178.
BRAMBELL, F. W. R., W. A. HEMMINGS, AND W. T. ROWLANDS. 1948.
The passage of antibodies from the maternal circulation into the
embryo in rabbits. Proceedings of the Royal Society of London, B.
Biological Sciences 135:390–403.
BRAUN, D. 1997. Die Milchkompositionen der Säugetiere im
Vergleich und die Milch des Menschen. Dissertation Doktor der
Naturwissenschaften, Universität Witten-Herdecke, Witten-Herdecke, Germany (in German).
BUSCHMANN, H. 1990. Infektionsabwehr. Pp. 30–37 in Neugeborenenund Säuglingskunde der Tiere (K. Walser and H. Bostedt, eds.).
Ferdinand Enke Verlag, Stuttgart, Germany (in German).
BUSS, D. H. 1968. Gross composition and variation of the components
of baboon milk during natural lactation. Journal of Nutrition
96:421–426.
BUTLER, J. E. 1974. Immunoglobulins of the mammary secretions.
Pp. 217–255 in Lactation. A comprehensive treatise (B. L. Larson
and V. Smith, eds.). Vol. 3. Academic Press, New York.
CLAUS, M. A., J. K. LEVY, K. MACDONALD, S. J. TUCKER, AND P. C.
CRAWFORD . 2006. Immunoglobulin concentrations in feline
colostrum and milk, and the requirement of colostrum for passive
transfer of immunity to neonatal kittens. Journal of Feline Medicine
and Surgery 8:184–191.
DAY, M. J. 2007. Immune system development in the dog and cat.
Journal of Comparative Pathology 137:810–815.
DOCUMENTA GEIGY. 1969. Wissenschaftliche Tabellen, 7. Aufl. J. R.
Geigy, Basel, Switzerland (in German).
EL-AGAMY, E. I. 2006. Camel milk. Pp. 297–344 in Handbook of milk
of non-bovine mammals (Y. W. Park and G. F. W. Haenlein, eds.).
Blackwell Publishing, Ames, Iowa.
ELSON, J., E. J. JENKINSON, AND W. D. BILLINGTON. 1975. Fc
receptors on mouse placenta and yolk sac cells. Nature 255:
412–414.
FERNÁNDEZ, F. M., ET AL. 1999. Composición del colostro y leche
de Corzuela (Mazama gouazoubira) (Artiodactyla, Cervidae).
Mastozoologı́a Neotropical 6:83–90 (in Spanish).
GASKIN, H. R., AND K. W. KELLEY. 1995. Immunology and neonatal
mortality. Pp. 39–55 in The neonatal pig. Development and survival
(M. A. Varley, ed.). CAB International, Wallingford, United
Kingdom.
GEISLER, J. H., AND Z. LUO. 1998. Cetaceans are highly derived
artiodactyls. Pp. 163–212 in The emergence of whales. Evolutionary
patterns in the origin of Cetacea (J. G. M. Thewissen, ed.). Plenum
Press, New York.
HARMS, C. A. 1993. Composition of prepartum mammary secretions
of two bowhead whales (Balaena mysticetus L.). Journal of Wildlife
Diseases 29:94–97.
HERRMANN, W. P., AND W. FORSTREUTER. 1967. Diaplacentare
Übertragung eines Paraproteins vom Typ cG. Klinische Wochenschrift 45:1035–1037 (in German).
JENKINSON, E. J., W. D. BILLINGTON, AND J. ELSON. 1976. Detection of
receptors for immunoglobulin on human placenta by EA rosette
formation. Clinical Experimental Immunology 23:456–461.
KACSKOVICS, I. 2004. Fc receptors in livestock species. Veterinary
Immunology and Immunopathology 102:351–362.
KARASOV, W. H., AND C. MARTÍNEZ DEL RIO. 2007. Physiological
ecology. How animals process energy, nutrients, and toxins.
Princeton University Press, Princeton, New Jersey.
KAUFMANN, P. 1990. Placentation und Placenta. Pp. 159–204 in
Humanembryologie. Lehrbuch und Atlas der vorgeburtlichen
April 2009
LANGER—COLOSTRUM, MILK, AND PASSIVE IMMUNITY
Entwicklung des Menschen (K. V. Hinrichsen, ed.). SpringerVerlag, Berlin, Germany (in German).
KEEN, L., B. LÖNNERDAL, M. CLEGG, AND L. S. HURLEY. 1981.
Developmental changes in composition of rat milk: trace elements,
minerals, protein, carbohydrate and fat. Journal of Nutrition
111:226–230.
KEEN, C. L., ET AL. 1982. Developmental changes in composition of
cats’ milk: trace elements, minerals, protein, carbohydrate and fat.
Journal of Nutrition 112:1763–1769.
LANGER, P. 2008a. The phases of maternal investment in eutherian
mammals. Zoology 111:148–162.
LANGER, P. 2008b. Mütter, Nachkommen, Ernährung. Eine Studie zur
frühen Ernährung höherer Säugetiere. Naturwissenschaftliche
Rundschau 61:61–67 (in German).
LASCELLES, A. K. 1979. The immune system of the ruminant
mammary gland and its role in the control of mastitis. Journal of
Dairy Science 62:154–160.
LIN, C.-T. 1980. Immunoelectron microscopic localization of
immunoglobulin G in human placenta. Journal of Histochemistry
and Cytochemistry 28:339–346.
LOCHMILLER, R. L., E. C. HELLGREN, W. E. GRANT, L. W. GREENE, AND
C. W. DILL. 1985. Description of collared peccary (Tayassu tajacu)
milk composition. Zoo Biology 4:375–379.
LÜLLMANN-RAUCH, R. 2003. Histologie. Georg Thieme Verlag,
Stuttgart, Germany (in German).
MALEK, A. 2003. Ex vivo human placenta models: transport of
immunoglobulin G and its subclasses. Vaccine 21:3362–3354.
MERAD, Z., AND A. E. WILD. 1992. The route of maternal IgM
transport to the rabbit fetus. Placenta 13:291–304.
MEYER, H., AND J. KAMPHUES. 1990. Grundlagen der Ernährung von
Neugeborenen. Pp. 55–71 in Neugeborenen- und Säuglingskunde
der Tiere (K. Walser and H. Bostedt, eds.). Ferdinand Enke Verlag,
Stuttgart, Germany (in German).
MILINKOVITCH, M. C., M. BÉRUBÉ AND P. J. PALSBØLL. 1998. Cetaceans
are highly derived artiodactyls. Pp. 113–131 in The emergence of
whales. Evolutionary patterns in the origin of Cetacea (J. G. M.
Thewissen, ed.). Plenum Press, New York.
MOSSMAN, H. W. 1987. Vertebrate fetal membranes. Comparative
ontogeny and morphology; evolution; phylogenetic significance;
basic functions; research opportunities. Macmillan Press, Basingstoke and London, United Kingdom.
OFTEDAL, O. T. 1984. Milk composition, milk yield and energy output
at peak lactation: a comparative review. Symposia of the Zoological
Society of London 51:33–85.
OSTHOFF, G., H. O. DE WAAL, A. HUGO, M. DE WIT, AND P. BOTES.
2005. Milk composition of a free-ranging African elephant
339
(Loxodonta africana) cow during early lactation. Comparative
Biochemistry and Physiology, A. Comparative Physiology
141:223–229.
PARK, Y. W. 2006a. Sow milk. Pp. 371–381 in Handbook of milk of
non-bovine mammals (Y. W. Park and G. F. W. Haenlein, eds.).
Blackwell Publishing, Ames, Iowa.
PARK, Y. W. 2006b. Minor species milk. Pp. 393–406 in Handbook of
milk of non-bovine mammals (Y. W. Park and G. F. W. Haenlein,
eds.). Blackwell Publishing, Ames, Iowa.
PARK, Y. W., AND G. F. W. HAENLEIN. 2006. Overview of milk of nonbovine mammals. Pp. 3–9 in Handbook of milk of non-bovine
mammals (Y. W. Park and G. F. W. Haenlein, eds.). Blackwell
Publishing, Ames, Iowa.
PLUSKE, J. R., I. H. WILLIAMS, AND F. X. AHERNE. 1995. Nutrition of
the neonatal pig. Pp. 187–235 in The neonatal pig. Development
and survival (M. A. Varley, ed.). CAB International, Wallingford,
United Kingdom.
ROOKE, J. A., ET AL. 2003. Relationships between passive absorption
of immunoglobulin G by the piglet and plasma concentrations of
immunoglobulin G at weaning. Livestock Production Science
81:223–234.
ROSENBERG, M. 2006. Llama milk. Pp. 383–391 in Handbook of milk
of non-bovine mammals (Y. W. Park and G. F. W. Haenlein, eds.).
Blackwell Publishing, Ames, Iowa.
SILK, T. M., M. GUO, G. F. W. HAENLEIN, AND Y. W. PARK. 2006. Yak
milk. Pp. 345–353 in Handbook of milk of non-bovine mammals
(Y. W. Park and G. F. W. Haenlein, eds.). Blackwell Publishing,
Ames, Iowa.
SOWLS, L. K. 1984. The peccaries. University of Arizona Press,
Tucson.
STOFFEL, M. H., A. E. FRIESS, AND S. H. HARTMANN. 2000. Ultrastructural evidence of transplacental transport of immunoglobulin
G in bitches. Journal of Reproduction and Fertility 118:315–326.
VERNIER, J. M., AND M.-F. SIRE. 1981. L’absorption intestinale des
protéines sous forme macromoléculaire chez les vertébrés. Implication physiologiques. Annales de Biologie 28:255–288 (in French).
WELSCH, U. 2003. Lehrbuch Histologie. Zytologie, Histologie,
Mikroskopische Anatomie. Urban & Fischer, München and Jena,
Germany (in German).
WILSON, D. E., AND D. M. REEDER (EDS.). 2005. Mammal species of
the world: a taxonomic and geographic reference. 3rd ed. Johns
Hopkins University Press, Baltimore, Maryland.
Submitted 19 February 2008. Accepted 30 May 2008.
Associate Editor was Fritz Geiser.